Microbial nitrogen dynamics in organic and mineral soil horizons along a latitudinal transect in western Siberia.

Soil N availability is constrained by the breakdown of N-containing polymers such as proteins to oligopeptides and amino acids that can be taken up by plants and microorganisms. Excess N is released from microbial cells as ammonium (N mineralization), which in turn can serve as substrate for nitrification. According to stoichiometric theory, N mineralization and nitrification are expected to increase in relation to protein depolymerization with decreasing N limitation, and thus from higher to lower latitudes and from topsoils to subsoils. To test these hypotheses, we compared gross rates of protein depolymerization, N mineralization and nitrification (determined using 15N pool dilution assays) in organic topsoil, mineral topsoil, and mineral subsoil of seven ecosystems along a latitudinal transect in western Siberia, from tundra (67°N) to steppe (54°N). The investigated ecosystems differed strongly in N transformation rates, with highest protein depolymerization and N mineralization rates in middle and southern taiga. All N transformation rates decreased with soil depth following the decrease in organic matter content. Related to protein depolymerization, N mineralization and nitrification were significantly higher in mineral than in organic horizons, supporting a decrease in microbial N limitation with depth. In contrast, we did not find indications for a decrease in microbial N limitation from arctic to temperate ecosystems along the transect. Our findings thus challenge the perception of ubiquitous N limitation at high latitudes, but suggest a transition from N to C limitation of microorganisms with soil depth, even in high-latitude systems such as tundra and boreal forest. KEY POINTS: We compared soil N dynamics of seven ecosystems along a latitudinal transectShifts in N dynamics suggest a decrease in microbial N limitation with depthWe found no decrease in microbial N limitation from arctic to temperate zones.

Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil.

Rising temperatures in the Arctic can affect soil organic matter (SOM) decomposition directly and indirectly, by increasing plant primary production and thus the allocation of plant-derived organic compounds into the soil. Such compounds, for example root exudates or decaying fine roots, are easily available for microorganisms, and can alter the decomposition of older SOM ("priming effect"). We here report on a SOM priming experiment in the active layer of a permafrost soil from the central Siberian Arctic, comparing responses of organic topsoil, mineral subsoil, and cryoturbated subsoil material (i.e., poorly decomposed topsoil material subducted into the subsoil by freeze-thaw processes) to additions of 13C-labeled glucose, cellulose, a mixture of amino acids, and protein (added at levels corresponding to approximately 1% of soil organic carbon). SOM decomposition in the topsoil was barely affected by higher availability of organic compounds, whereas SOM decomposition in both subsoil horizons responded strongly. In the mineral subsoil, SOM decomposition increased by a factor of two to three after any substrate addition (glucose, cellulose, amino acids, protein), suggesting that the microbial decomposer community was limited in energy to break down more complex components of SOM. In the cryoturbated horizon, SOM decomposition increased by a factor of two after addition of amino acids or protein, but was not significantly affected by glucose or cellulose, indicating nitrogen rather than energy limitation. Since the stimulation of SOM decomposition in cryoturbated material was not connected to microbial growth or to a change in microbial community composition, the additional nitrogen was likely invested in the production of extracellular enzymes required for SOM decomposition. Our findings provide a first mechanistic understanding of priming in permafrost soils and suggest that an increase in the availability of organic carbon or nitrogen, e.g., by increased plant productivity, can change the decomposition of SOM stored in deeper layers of permafrost soils, with possible repercussions on the global climate.

Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile.

Current knowledge of the mechanisms driving soil organic matter (SOM) turnover and responses to warming is mainly limited to surface soils, although over 50% of global soil carbon is contained in subsoils. Deep soils have different physicochemical properties, nutrient inputs, and microbiomes, which may harbor distinct functional traits and lead to different SOM dynamics and temperature responses. We hypothesized that kinetic and thermal properties of soil exoenzymes, which mediate SOM depolymerization, vary with soil depth, reflecting microbial adaptation to distinct substrate and temperature regimes. We determined the Michaelis-Menten (MM) kinetics of three ubiquitous enzymes involved in carbon (C), nitrogen (N) and phosphorus (P) acquisition at six soil depths down to 90 cm at a temperate forest, and their temperature sensitivity based on Arrhenius/Q 10 and Macromolecular Rate Theory (MMRT) models over six temperatures between 4-50°C. Maximal enzyme velocity (V max) decreased strongly with depth for all enzymes, both on a dry soil mass and a microbial biomass C basis, whereas their affinities increased, indicating adaptation to lower substrate availability. Surprisingly, microbial biomass-specific catalytic efficiencies also decreased with depth, except for the P-acquiring enzyme, indicating distinct nutrient demands at depth relative to microbial abundance. These results suggested that deep soil microbiomes encode enzymes with intrinsically lower turnover and/or produce less enzymes per cell, reflecting distinct life strategies. The relative kinetics between different enzymes also varied with depth, suggesting an increase in relative P demand with depth, or that phosphatases may be involved in C acquisition. V max and catalytic efficiency increased consistently with temperature for all enzymes, leading to overall higher SOM-decomposition potential, but enzyme temperature sensitivity was similar at all depths and between enzymes, based on both Arrhenius/Q 10 and MMRT models. In a few cases, however, temperature affected differently the kinetic properties of distinct enzymes at discrete depths, suggesting that it may alter the relative depolymerization of different compounds. We show that soil exoenzyme kinetics may reflect intrinsic traits of microbiomes adapted to distinct soil depths, although their temperature sensitivity is remarkably uniform. These results improve our understanding of critical mechanisms underlying SOM dynamics and responses to changing temperatures through the soil profile.

Ammonia Oxidation by the Arctic Terrestrial Thaumarchaeote Candidatus Nitrosocosmicus arcticus Is Stimulated by Increasing Temperatures.

Climate change is causing arctic regions to warm disproportionally faster than those at lower latitudes, leading to alterations in carbon and nitrogen cycling, and potentially higher greenhouse gas emissions. It is thus increasingly important to better characterize the microorganisms driving arctic biogeochemical processes and their potential responses to changing conditions. Here, we describe a novel thaumarchaeon enriched from an arctic soil, Candidatus Nitrosocosmicus arcticus strain Kfb, which has been maintained for seven years in stable laboratory enrichment cultures as an aerobic ammonia oxidizer, with ammonium or urea as substrates. Genomic analyses show that this organism harbors all genes involved in ammonia oxidation and in carbon fixation via the 3-hydroxypropionate/4-hydroxybutyrate cycle, characteristic of all AOA, as well as the capability for urea utilization and potentially also for heterotrophic metabolism, similar to other AOA. Ca. N. arcticus oxidizes ammonia optimally between 20 and 28°C, well above average temperatures in its native high arctic environment (-13-4°C). Ammonia oxidation rates were nevertheless much lower than those of most cultivated mesophilic AOA (20-45°C). Intriguingly, we repeatedly observed apparent faster growth rates (based on marker gene counts) at lower temperatures (4-8°C) but without detectable nitrite production. Together with potential metabolisms predicted from its genome content, these observations indicate that Ca. N. arcticus is not a strict chemolithotrophic ammonia oxidizer and add to cumulating evidence for a greater metabolic and physiological versatility of AOA. The physiology of Ca. N. arcticus suggests that increasing temperatures might drastically affect nitrification in arctic soils by stimulating archaeal ammonia oxidation.

Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes.

Ammonia-oxidising archaea (AOA) are ubiquitous and abundant in nature and play a major role in nitrogen cycling. AOA have been studied intensively based on the amoA gene (encoding ammonia monooxygenase subunit A), making it the most sequenced functional marker gene. Here, based on extensive phylogenetic and meta-data analyses of 33,378 curated archaeal amoA sequences, we define a highly resolved taxonomy and uncover global environmental patterns that challenge many earlier generalisations. Particularly, we show: (i) the global frequency of AOA is extremely uneven, with few clades dominating AOA diversity in most ecosystems; (ii) characterised AOA do not represent most predominant clades in nature, including soils and oceans; (iii) the functional role of the most prevalent environmental AOA clade remains unclear; and (iv) AOA harbour molecular signatures that possibly reflect phenotypic traits. Our work synthesises information from a decade of research and provides the first integrative framework to study AOA in a global context.

Drying and Rainfall Shape the Structure and Functioning of Nitrifying Microbial Communities in Riverbed Sediments.

Non-flow periods in fluvial ecosystems are a global phenomenon. Streambed drying and rewetting by sporadic rainfalls could drive considerable changes in the microbial communities that govern stream nitrogen (N) availability at different temporal and spatial scales. We performed a microcosm-based experiment to investigate how dry period duration (DPD) (0, 3, 6, and 9 weeks) and magnitude of sporadic rewetting by rainfall (0, 4, and 21 mm applied at end of dry period) affected stocks of N in riverbed sediments, ammonia-oxidizing bacteria (AOB) and archaea (AOA) and rates of ammonia oxidation (AO), and emissions of nitrous oxide (N2O) to the atmosphere. While ammonium (NH4 +) pool size decreased, nitrate (NO3 -) pool size increased in sediments with progressive drying. Concomitantly, the relative and absolute abundance of AOB and, especially, AOA (assessed by 16S rRNA gene sequencing and quantitative PCR of ammonia monooxygenase genes) increased, despite an apparent decrease of AO rates with drying. An increase of N2O emissions occurred at early drying before substantially dropping until the end of the experiment. Strong rainfall of 21 mm increased AO rates and NH4 + in sediments, whereas modest rainfall of 4 mm triggered a notable increase of N2O fluxes. Interestingly, such responses were detected only after 6 and 9 weeks of drying. Our results demonstrate that progressive drying drives considerable changes in in-stream N cycling and the associated nitrifying microbial communities, and that sporadic rainfall can modulate these effects. Our findings are particularly relevant for N processing and transport in rivers with alternating dry and wet phases - a hydrological scenario expected to become more important in the future.

Plant-derived compounds stimulate the decomposition of organic matter in arctic permafrost soils.

Arctic ecosystems are warming rapidly, which is expected to promote soil organic matter (SOM) decomposition. In addition to the direct warming effect, decomposition can also be indirectly stimulated via increased plant productivity and plant-soil C allocation, and this so called "priming effect" might significantly alter the ecosystem C balance. In this study, we provide first mechanistic insights into the susceptibility of SOM decomposition in arctic permafrost soils to priming. By comparing 119 soils from four locations across the Siberian Arctic that cover all horizons of active layer and upper permafrost, we found that an increased availability of plant-derived organic C particularly stimulated decomposition in subsoil horizons where most of the arctic soil carbon is located. Considering the 1,035 Pg of arctic soil carbon, such an additional stimulation of decomposition beyond the direct temperature effect can accelerate net ecosystem C losses, and amplify the positive feedback to global warming.

Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea.

The functioning of Arctic soil ecosystems is crucially important for global climate, and basic knowledge regarding their biogeochemical processes is lacking. Nitrogen (N) is the major limiting nutrient in these environments, and its availability is strongly dependent on nitrification. However, microbial communities driving this process remain largely uncharacterized in Arctic soils, namely those catalyzing the rate-limiting step of ammonia (NH3) oxidation. Eleven Arctic soils were analyzed through a polyphasic approach, integrating determination of gross nitrification rates, qualitative and quantitative marker gene analyses of ammonia-oxidizing archaea (AOA) and bacteria (AOB) and enrichment of AOA in laboratory cultures. AOA were the only NH3 oxidizers detected in five out of 11 soils and outnumbered AOB in four of the remaining six soils. The AOA identified showed great phylogenetic diversity and a multifactorial association with the soil properties, reflecting an overall distribution associated with tundra type and with several physico-chemical parameters combined. Remarkably, the different gross nitrification rates between soils were associated with five distinct AOA clades, representing the great majority of known AOA diversity in soils, which suggests differences in their nitrifying potential. This was supported by selective enrichment of two of these clades in cultures with different NH3 oxidation rates. In addition, the enrichments provided the first direct evidence for NH3 oxidation by an AOA from an uncharacterized Thaumarchaeota-AOA lineage. Our results indicate that AOA are functionally heterogeneous and that the selection of distinct AOA populations by the environment can be a determinant for nitrification activity and N availability in soils.